Ultrafast XANES Monitors Femtosecond Sequential Structural Evolution in Photoexcited Coenzyme B12
Abstract
Polarized X-ray absorption near-edge structure (XANES) at the Co K-edge and broadband UV-vis transient absorption are used to monitor the sequential evolution of the excited-state structure of coenzyme B12 (adenosylcobalamin) over the first picosecond following excitation. The initial state is characterized by sub-100 fs sequential changes around the central cobalt. These are polarized first in the y-direction orthogonal to the transition dipole and 50 fs later in the x-direction along the transition dipole. Expansion of the axial bonds follows on a ca. 200 fs time scale as the molecule moves out of the Franck-Condon active region of the potential energy surface. On the same 200 fs time scale there are electronic changes that result in the loss of stimulated emission and the appearance of a strong absorption at 340 nm. These measurements provide a cobalt-centered movie of the excited molecule as it evolves to the local excited-state minimum.
- Authors:
-
[1];
[2];
[4];
[6];
[4];
[4];
[7]
- Univ. of Michigan, Ann Arbor, MI (United States). Dept. of Chemistry
- Univ. of Michigan, Ann Arbor, MI (United States). Dept. of Physics
- SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source (LCLS)
- Univ. of Michigan, Ann Arbor, MI (United States). Dept. of Chemistry and Dept. of Biophysics
- Univ. of Michigan, Ann Arbor, MI (United States). Applied Physics Program
- Univ. of Louisville, KY (United States). Dept. of Chemistry
- Univ. of Michigan, Ann Arbor, MI (United States). Dept. of Chemistry, Dept. of Physics, and Dept. of Biophysics
- Publication Date:
- Research Org.:
- SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1605287
- Grant/Contract Number:
- AC02-76SF00515; 1464584; 1565795; 1836435
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry
- Additional Journal Information:
- Journal Volume: 124; Journal Issue: 1; Journal ID: ISSN 1520-6106
- Publisher:
- American Chemical Society
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; X-ray absorption near edge spectroscopy; X-rays; Light absorption; Absorption; Oscillation
Citation Formats
Miller, Nicholas A., Michocki, Lindsay B., Konar, Arkaprabha, Alonso-Mori, Roberto, Deb, Aniruddha, Glownia, James M., Sofferman, Danielle L., Song, Sanghoon, Kozlowski, Pawel M., Kubarych, Kevin J., Penner-Hahn, James E., and Sension, Roseanne J. Ultrafast XANES Monitors Femtosecond Sequential Structural Evolution in Photoexcited Coenzyme B12. United States: N. p., 2019.
Web. doi:10.1021/acs.jpcb.9b09286.
Miller, Nicholas A., Michocki, Lindsay B., Konar, Arkaprabha, Alonso-Mori, Roberto, Deb, Aniruddha, Glownia, James M., Sofferman, Danielle L., Song, Sanghoon, Kozlowski, Pawel M., Kubarych, Kevin J., Penner-Hahn, James E., & Sension, Roseanne J. Ultrafast XANES Monitors Femtosecond Sequential Structural Evolution in Photoexcited Coenzyme B12. United States. https://doi.org/10.1021/acs.jpcb.9b09286
Miller, Nicholas A., Michocki, Lindsay B., Konar, Arkaprabha, Alonso-Mori, Roberto, Deb, Aniruddha, Glownia, James M., Sofferman, Danielle L., Song, Sanghoon, Kozlowski, Pawel M., Kubarych, Kevin J., Penner-Hahn, James E., and Sension, Roseanne J. Wed .
"Ultrafast XANES Monitors Femtosecond Sequential Structural Evolution in Photoexcited Coenzyme B12". United States. https://doi.org/10.1021/acs.jpcb.9b09286. https://www.osti.gov/servlets/purl/1605287.
@article{osti_1605287,
title = {Ultrafast XANES Monitors Femtosecond Sequential Structural Evolution in Photoexcited Coenzyme B12},
author = {Miller, Nicholas A. and Michocki, Lindsay B. and Konar, Arkaprabha and Alonso-Mori, Roberto and Deb, Aniruddha and Glownia, James M. and Sofferman, Danielle L. and Song, Sanghoon and Kozlowski, Pawel M. and Kubarych, Kevin J. and Penner-Hahn, James E. and Sension, Roseanne J.},
abstractNote = {Polarized X-ray absorption near-edge structure (XANES) at the Co K-edge and broadband UV-vis transient absorption are used to monitor the sequential evolution of the excited-state structure of coenzyme B12 (adenosylcobalamin) over the first picosecond following excitation. The initial state is characterized by sub-100 fs sequential changes around the central cobalt. These are polarized first in the y-direction orthogonal to the transition dipole and 50 fs later in the x-direction along the transition dipole. Expansion of the axial bonds follows on a ca. 200 fs time scale as the molecule moves out of the Franck-Condon active region of the potential energy surface. On the same 200 fs time scale there are electronic changes that result in the loss of stimulated emission and the appearance of a strong absorption at 340 nm. These measurements provide a cobalt-centered movie of the excited molecule as it evolves to the local excited-state minimum.},
doi = {10.1021/acs.jpcb.9b09286},
journal = {Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry},
number = 1,
volume = 124,
place = {United States},
year = {Wed Dec 18 00:00:00 EST 2019},
month = {Wed Dec 18 00:00:00 EST 2019}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 13 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Simplicity Beneath Complexity: Counting Molecular Electrons Reveals Transients and Kinetics of Photodissociation Reactions
journal, April 2019
- Ruddock, Jennifer M.; Zotev, Nikola; Stankus, Brian
- Angewandte Chemie International Edition, Vol. 58, Issue 19
Fundamental Limits on Spatial Resolution in Ultrafast X-ray Diffraction
journal, May 2017
- Kirrander, Adam; Weber, Peter
- Applied Sciences, Vol. 7, Issue 6
Femtosecond photodissociation dynamics of 1,4-diiodobenzene by gas-phase X-ray scattering and photoelectron spectroscopy
journal, January 2016
- Stankus, Brian; Budarz, James M.; Kirrander, Adam
- Faraday Discussions, Vol. 194
Observation of femtosecond molecular dynamics via pump–probe gas phase x-ray scattering
journal, January 2016
- Budarz, J. M.; Minitti, M. P.; Cofer-Shabica, D. V.
- Journal of Physics B: Atomic, Molecular and Optical Physics, Vol. 49, Issue 3
Ultrafast structural dynamics of photo-reactions observed by time-resolved x-ray cross-correlation analysis
journal, March 2019
- Vester, Peter; Zaluzhnyy, Ivan A.; Kurta, Ruslan P.
- Structural Dynamics, Vol. 6, Issue 2
Initial metal–metal bond breakage detected by fs X-ray scattering in the photolysis of Ru 3 (CO) 12 in cyclohexane at 400 nm
journal, January 2019
- Kong, Q. Y.; Laursen, M. G.; Haldrup, K.
- Photochemical & Photobiological Sciences, Vol. 18, Issue 2
Ultrafast X-Ray Scattering Measurements of Coherent Structural Dynamics on the Ground-State Potential Energy Surface of a Diplatinum Molecule
journal, February 2019
- Haldrup, Kristoffer; Levi, Gianluca; Biasin, Elisa
- Physical Review Letters, Vol. 122, Issue 6
Anisotropy enhanced X-ray scattering from solvated transition metal complexes
journal, February 2018
- Biasin, Elisa; van Driel, Tim B.; Levi, Gianluca
- Journal of Synchrotron Radiation, Vol. 25, Issue 2
Atomistic characterization of the active-site solvation dynamics of a model photocatalyst
journal, November 2016
- van Driel, Tim B.; Kjær, Kasper S.; Hartsock, Robert W.
- Nature Communications, Vol. 7, Issue 1
Ultrafast X-Ray Crystallography and Liquidography
journal, May 2017
- Ki, Hosung; Oang, Key Young; Kim, Jeongho
- Annual Review of Physical Chemistry, Vol. 68, Issue 1
Ultrafast X-ray scattering reveals vibrational coherence following Rydberg excitation
journal, July 2019
- Stankus, Brian; Yong, Haiwang; Zotev, Nikola
- Nature Chemistry, Vol. 11, Issue 8
Probing the Excited State of Methylcobalamin Using Polarized Time-Resolved X-ray Absorption Spectroscopy
journal, June 2019
- Michocki, Lindsay B.; Miller, Nicholas A.; Alonso-Mori, Roberto
- The Journal of Physical Chemistry B, Vol. 123, Issue 28
Ultrafast X-ray Absorption Near Edge Structure Reveals Ballistic Excited State Structural Dynamics
journal, May 2018
- Miller, Nicholas A.; Deb, Aniruddha; Alonso-Mori, Roberto
- The Journal of Physical Chemistry A, Vol. 122, Issue 22
Polarized XANES Monitors Femtosecond Structural Evolution of Photoexcited Vitamin B 12
journal, January 2017
- Miller, Nicholas A.; Deb, Aniruddha; Alonso-Mori, Roberto
- Journal of the American Chemical Society, Vol. 139, Issue 5
Ligand manipulation of charge transfer excited state relaxation and spin crossover in [Fe(2,2′-bipyridine) 2 (CN) 2 ]
journal, July 2017
- Kjær, Kasper S.; Zhang, Wenkai; Alonso-Mori, Roberto
- Structural Dynamics, Vol. 4, Issue 4
Solvent control of charge transfer excited state relaxation pathways in [Fe(2,2′-bipyridine)(CN) 4 ] 2−
journal, January 2018
- Kjær, Kasper S.; Kunnus, Kristjan; Harlang, Tobias C. B.
- Physical Chemistry Chemical Physics, Vol. 20, Issue 6
Ultrafast Excited State Relaxation of a Metalloporphyrin Revealed by Femtosecond X-ray Absorption Spectroscopy
journal, July 2016
- Shelby, Megan L.; Lestrange, Patrick J.; Jackson, Nicholas E.
- Journal of the American Chemical Society, Vol. 138, Issue 28
Butterfly Deformation Modes in a Photoexcited Pyrazolate-Bridged Pt Complex Measured by Time-Resolved X-Ray Scattering in Solution
journal, September 2016
- Haldrup, Kristoffer; Dohn, Asmus O.; Shelby, Megan L.
- The Journal of Physical Chemistry A, Vol. 120, Issue 38
Imaging ultrafast excited state pathways in transition metal complexes by X-ray transient absorption and scattering using X-ray free electron laser source
journal, January 2016
- Chen, Lin X.; Shelby, Megan L.; Lestrange, Patrick J.
- Faraday Discussions, Vol. 194
Recent advances on ultrafast X-ray spectroscopy in the chemical sciences
journal, January 2014
- Chen, L. X.; Zhang, X.; Shelby, M. L.
- Chem. Sci., Vol. 5, Issue 11
Observing heme doming in myoglobin with femtosecond X-ray absorption spectroscopya)
journal, May 2015
- Levantino, M.; Lemke, H. T.; Schirò, G.
- Structural Dynamics, Vol. 2, Issue 4
Resolving structures of transition metal complex reaction intermediates with femtosecond EXAFS
journal, January 2020
- Britz, Alexander; Abraham, Baxter; Biasin, Elisa
- Physical Chemistry Chemical Physics, Vol. 22, Issue 5
Tracking multiple components of a nuclear wavepacket in photoexcited Cu(I)-phenanthroline complex using ultrafast X-ray spectroscopy
journal, August 2019
- Katayama, Tetsuo; Northey, Thomas; Gawelda, Wojciech
- Nature Communications, Vol. 10, Issue 1
Adenosylcobalamin enzymes: Theory and experiment begin to converge
journal, November 2012
- Marsh, E. Neil G.; Meléndez, Gabriel D. Román
- Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1824, Issue 11
Adenosyl Radical: Reagent and Catalyst in Enzyme Reactions
journal, February 2010
- Marsh, E. Neil G.; Patterson, Dustin P.; Li, Lei
- ChemBioChem, Vol. 11, Issue 5
The Many Faces of Vitamin B12: Catalysis by Cobalamin-Dependent Enzymes
journal, June 2003
- Banerjee, Ruma; Ragsdale, Stephen W.
- Annual Review of Biochemistry, Vol. 72, Issue 1, p. 209-247
Vitamin B 12 in the spotlight again
journal, April 2017
- Bridwell-Rabb, Jennifer; Drennan, Catherine L.
- Current Opinion in Chemical Biology, Vol. 37
Vitamin B 12 catalysed reactions
journal, January 2015
- Giedyk, Maciej; Goliszewska, Katarzyna; Gryko, Dorota
- Chemical Society Reviews, Vol. 44, Issue 11
A New Facet of Vitamin B 12 : Gene Regulation by Cobalamin-Based Photoreceptors
journal, June 2017
- Padmanabhan, S.; Jost, Marco; Drennan, Catherine L.
- Annual Review of Biochemistry, Vol. 86, Issue 1
The photochemical mechanism of a B12-dependent photoreceptor protein
journal, August 2015
- Kutta, Roger J.; Hardman, Samantha J. O.; Johannissen, Linus O.
- Nature Communications, Vol. 6, Issue 1
Structural basis for gene regulation by a B12-dependent photoreceptor
journal, September 2015
- Jost, Marco; Fernández-Zapata, Jésus; Polanco, María Carmen
- Nature, Vol. 526, Issue 7574
Light-dependent gene regulation by a coenzyme B12-based photoreceptor
journal, April 2011
- Ortiz-Guerrero, J. M.; Polanco, M. C.; Murillo, F. J.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 18
Vitamin B12 partners the CarH repressor to downregulate a photoinducible promoter in Myxococcus xanthus: Light-inducible promoter control by B12 and CarH
journal, December 2007
- Pérez-Marín, Mari Cruz; Padmanabhan, S.; Polanco, María Carmen
- Molecular Microbiology, Vol. 67, Issue 4
Vitamin B 12 : A Tunable, Long Wavelength, Light-Responsive Platform for Launching Therapeutic Agents
journal, October 2015
- Shell, Thomas A.; Lawrence, David S.
- Accounts of Chemical Research, Vol. 48, Issue 11
Tunable Visible and Near-IR Photoactivation of Light-Responsive Compounds by Using Fluorophores as Light-Capturing Antennas
journal, November 2013
- Shell, Thomas A.; Shell, Jennifer R.; Rodgers, Zachary L.
- Angewandte Chemie International Edition, Vol. 53, Issue 3
Synthesis, characterization and cellular location of cytotoxic constitutional organometallic isomers of rhenium delivered on a cyanocobalmin scaffold
journal, January 2015
- Santoro, Giuseppe; Zlateva, Theodora; Ruggi, Albert
- Dalton Transactions, Vol. 44, Issue 15
Photolytic properties of the biologically active forms of vitamin B12
journal, April 2019
- Toda, Megan J.; Lodowski, Piotr; Mamun, Abdullah Al
- Coordination Chemistry Reviews, Vol. 385
Photolytic Properties of Antivitamins B 12
journal, June 2018
- Lodowski, Piotr; Toda, Megan J.; Ciura, Karolina
- Inorganic Chemistry, Vol. 57, Issue 13
Mechanism of the photo-induced activation of Co C bond in methylcobalamin-dependent methionine synthase
journal, December 2018
- Ghosh, Arghya Pratim; Mamun, Abdullah Al; Lodowski, Piotr
- Journal of Photochemistry and Photobiology B: Biology, Vol. 189
Photolytic properties of cobalamins: a theoretical perspective
journal, January 2016
- Kozlowski, Pawel M.; Garabato, Brady D.; Lodowski, Piotr
- Dalton Transactions, Vol. 45, Issue 11
Mechanism of Co–C photodissociation in adenosylcobalamin
journal, January 2016
- Garabato, Brady D.; Lodowski, Piotr; Jaworska, Maria
- Physical Chemistry Chemical Physics, Vol. 18, Issue 28
The X-ray Pump–Probe instrument at the Linac Coherent Light Source
journal, April 2015
- Chollet, Matthieu; Alonso-Mori, Roberto; Cammarata, Marco
- Journal of Synchrotron Radiation, Vol. 22, Issue 3
Antivitamins B 12 in a Microdrop: The Excited-State Structure of a Precious Sample Using Transient Polarized X-ray Absorption Near-Edge Structure
journal, August 2019
- Miller, Nicholas A.; Michocki, Lindsay B.; Alonso-Mori, Roberto
- The Journal of Physical Chemistry Letters, Vol. 10, Issue 18
XAS spectroscopy reveals X-ray-induced photoreduction of free and protein-bound B 12 cofactors
journal, July 2000
- Champloy, Frederic; Gruber, Karl; Jogl, Gerwald
- Journal of Synchrotron Radiation, Vol. 7, Issue 4
Accurate Redetermination of the X-ray Structure and Electronic Bonding in Adenosylcobalamin
journal, January 2004
- Ouyang, Lizhi; Rulis, Paul; Ching, W. Y.
- Inorganic Chemistry, Vol. 43, Issue 4
DFT Analysis of Co−Alkyl and Co−Adenosyl Vibrational Modes in B 12 -Cofactors
journal, June 2006
- Kozlowski, Pawel M.; Andruniow, Tadeusz; Jarzecki, Andrzej A.
- Inorganic Chemistry, Vol. 45, Issue 14
Vibrational Analysis of Methylcobalamin
journal, January 2002
- Andruniow, Tadeusz; Zgierski, Marek Z.; Kozlowski, Pawel M.
- The Journal of Physical Chemistry A, Vol. 106, Issue 7
Vibrational Assignment and Definite Harmonic Force Field for Porphine. 2. Comparison with Nonresonance Raman Data
journal, January 1996
- Kozlowski, Pawel M.; Jarzȩcki, Andrzej A.; Pulay, Peter
- The Journal of Physical Chemistry, Vol. 100, Issue 33
Vibrational Assignment and Definite Harmonic Force Field for Porphine. 1. Scaled Quantum Mechanical Results and Comparison with Empirical Force Field
journal, January 1996
- Kozlowski, Pawel M.; Jarzȩcki, Andrzej A.; Pulay, Peter
- The Journal of Physical Chemistry, Vol. 100, Issue 17
Self-consistent aspects of x-ray absorption calculations
journal, August 2009
- Bunău, O.; Joly, Y.
- Journal of Physics: Condensed Matter, Vol. 21, Issue 34
X-ray absorption near-edge structure calculations beyond the muffin-tin approximation
journal, March 2001
- Joly, Y.
- Physical Review B, Vol. 63, Issue 12
Spectroscopic and Computational Studies of Co 3+ -Corrinoids: Spectral and Electronic Properties of the B 12 Cofactors and Biologically Relevant Precursors
journal, May 2003
- Stich, Troy A.; Brooks, Amanda J.; Buan, Nicole R.
- Journal of the American Chemical Society, Vol. 125, Issue 19
Femtosecond spectroscopy of condensed phases with chirped supercontinuum probing
journal, March 1999
- Kovalenko, S. A.; Dobryakov, A. L.; Ruthmann, J.
- Physical Review A, Vol. 59, Issue 3
Time-Resolved Spectroscopic Studies of B 12 Coenzymes: A Comparison of the Primary Photolysis Mechanism in Methyl-, Ethyl-, n -Propyl-, and 5‘-Deoxyadenosylcobalamin
journal, January 2002
- Cole, Allwyn G.; Yoder, Laurie M.; Shiang, Joseph J.
- Journal of the American Chemical Society, Vol. 124, Issue 3
Local environment of metal ions in phthalocyanines: K-edge X-ray absorption spectra
journal, January 2016
- Rossi, G.; d'Acapito, F.; Amidani, L.
- Physical Chemistry Chemical Physics, Vol. 18, Issue 34
Axial Ligation and Redox Changes at the Cobalt Ion in Cobalamin Bound to Corrinoid Iron-Sulfur Protein (CoFeSP) or in Solution Characterized by XAS and DFT
journal, July 2016
- Schrapers, Peer; Mebs, Stefan; Goetzl, Sebastian
- PLOS ONE, Vol. 11, Issue 7
Influence of Environment on the Electronic Structure of Cob(III)alamins: Time-Resolved Absorption Studies of the S 1 State Spectrum and Dynamics
journal, June 2007
- Harris, D. Ahmasi; Stickrath, Andrew B.; Carroll, Elizabeth C.
- Journal of the American Chemical Society, Vol. 129, Issue 24
Time-Resolved Spectroscopic Studies of B 12 Coenzymes: The Photolysis of Methylcobalamin Is Wavelength Dependent
journal, November 1999
- Shiang, Joseph J.; Walker, Larry A.; Anderson, Neil A.
- The Journal of Physical Chemistry B, Vol. 103, Issue 47
Time-Resolved Spectroscopic Studies of B 12 Coenzymes: The Identification of a Metastable Cob(III)alamin Photoproduct in the Photolysis of Methylcobalamin
journal, April 1998
- Walker, Larry A.; Jarrett, Joseph T.; Anderson, Neil A.
- Journal of the American Chemical Society, Vol. 120, Issue 15
Photodissociation of Co−C Bond in Methyl- and Ethylcobalamin: An Insight from TD-DFT Calculations
journal, April 2009
- Lodowski, Piotr; Jaworska, Maria; Andruniów, Tadeusz
- The Journal of Physical Chemistry B, Vol. 113, Issue 19
Mechanism of Co–C Bond Photolysis in the Base-On Form of Methylcobalamin
journal, December 2014
- Lodowski, Piotr; Jaworska, Maria; Andruniów, Tadeusz
- The Journal of Physical Chemistry A, Vol. 118, Issue 50
Vibrational Coherence Spectroscopy of the Heme Domain in the CO-Sensing Transcriptional Activator CooA
journal, November 2011
- Karunakaran, Venugopal; Benabbas, Abdelkrim; Youn, Hwan
- Journal of the American Chemical Society, Vol. 133, Issue 46
Investigations of Low-Frequency Vibrational Dynamics and Ligand Binding Kinetics of Cystathionine β-Synthase
journal, February 2010
- Karunakaran, Venugopal; Benabbas, Abdelkrim; Sun, Yuhan
- The Journal of Physical Chemistry B, Vol. 114, Issue 9
Spectroscopic identification of reactive porphyrin motions
journal, July 2011
- Barabanschikov, Alexander; Demidov, Alexander; Kubo, Minoru
- The Journal of Chemical Physics, Vol. 135, Issue 1
Femtosecond Stimulated Raman Exposes the Role of Vibrational Coherence in Condensed-Phase Photoreactivity
journal, March 2016
- Hoffman, David P.; Mathies, Richard A.
- Accounts of Chemical Research, Vol. 49, Issue 4
Vibronic and Vibrational Coherences in Two-Dimensional Electronic Spectra of Supramolecular J-Aggregates
journal, March 2013
- Milota, Franz; Prokhorenko, Valentyn I.; Mancal, Tomas
- The Journal of Physical Chemistry A, Vol. 117, Issue 29
Coherence Spectroscopy in the Condensed Phase: Insights into Molecular Structure, Environment, and Interactions
journal, October 2017
- Dean, Jacob C.; Scholes, Gregory D.
- Accounts of Chemical Research, Vol. 50, Issue 11